Neurons in the monkey frontopolar cortex encode learning stage and goal during a fast learning task.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
16 Feb 2024
Historique:
received: 22 07 2023
accepted: 17 01 2024
medline: 16 2 2024
pubmed: 16 2 2024
entrez: 16 2 2024
Statut: aheadofprint

Résumé

The frontopolar cortex (FPC) is, to date, one of the least understood regions of the prefrontal cortex. The current understanding of its function suggests that it plays a role in the control of exploratory behaviors by coordinating the activities of other prefrontal cortex areas involved in decision-making and exploiting actions based on their outcomes. Based on this hypothesis, FPC would drive fast-learning processes through a valuation of the different alternatives. In our study, we used a modified version of a well-known paradigm, the object-in-place (OIP) task, to test this hypothesis in electrophysiology. This paradigm is designed to maximize learning, enabling monkeys to learn in one trial, which is an ability specifically impaired after a lesion of the FPC. We showed that FPC neurons presented an extremely specific pattern of activity by representing the learning stage, exploration versus exploitation, and the goal of the action. However, our results do not support the hypothesis that neurons in the frontal pole compute an evaluation of different alternatives. Indeed, the position of the chosen target was strongly encoded at its acquisition, but the position of the unchosen target was not. Once learned, this representation was also found at the problem presentation, suggesting a monitoring activity of the synthetic goal preceding its acquisition. Our results highlight important features of FPC neurons in fast-learning processes without confirming its role in the disengagement of cognitive control from the current goals.

Identifiants

pubmed: 38363801
doi: 10.1371/journal.pbio.3002500
pii: PBIOLOGY-D-23-01851
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3002500

Informations de copyright

Copyright: © 2024 Nougaret et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Auteurs

Simon Nougaret (S)

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.

Lorenzo Ferrucci (L)

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.

Francesco Ceccarelli (F)

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.
PhD program in Behavioral Neuroscience, Sapienza University of Rome, Rome, Italy.

Stefano Sacchetti (S)

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.

Danilo Benozzo (D)

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.

Valeria Fascianelli (V)

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.

Richard C Saunders (RC)

Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland, United States of America.

Luc Renaud (L)

Institut de Neurosciences de la Timone, UMR7289, Centre National de la Recherche Scientifique and Aix-Marseille Université, Marseille, France.

Aldo Genovesio (A)

Department of Physiology and Pharmacology, Sapienza University of Rome, Rome, Italy.

Classifications MeSH